Plant Ecol (2018) 219:1197–1207

https://doi.org/10.1007/s11258-018-0872-9 (0123456789().,-volV)(0123456789().,-volV)

The seeds of success: release from fungal attack on seeds may influence the invasiveness of alien Impatiens

Kamil Najberek . Wojciech Pusz . Wojciech Solarz . Pawel Olejniczak

Received: 8 May 2018 / Accepted: 16 August 2018 / Published online: 23 August 2018 Ó The Author(s) 2018

Abstract Although closely related, Impatiens glan- pathogens (Cladosporium cladosporioides, Alternaria dulifera and Impatiens balfourii differ in their inva- alternata) correlated negatively with the number of siveness in Europe; only the former is highly invasive colonies of true pathogens; we suggest that the there. Following the assumptions of the enemy release secondary pathogens may have prevented the occur- hypothesis (ERH), we tested whether these differences rence of the true pathogens. The reason for the may be explained by the levels of seed infestation by between-country differences in the fungal pathogen pathogenic fungi. Using seeds collected along the communities is unclear. A possible explanation is that Swiss-Italian border, we recorded four true pathogens Italy and Switzerland differ in their road and green- of seeds: Fusarium culmorum, F. oxysporum, F. area maintenance work schemes, which may have sporotrichoides, and Giberella avenacea. In Italy the influenced pathogen pressure on seeds. This study is seeds of I. balfourii were infected by fungal pathogens one of the few that offers results indicating that release more often than those of I. glandulifera, while in from enemies may be crucial to the invasion success of Switzerland both species were under the same level of plants as early as the seed stage. pressure. However, the overall differences in pathogen abundance were consistent with the ERH: seeds of the Keywords Biological invasions Á Seed enemies Á more invasive species were attacked less. This could Seedborne fungi Á Seed antagonists Á Obligatory be a result of differences between the communities of pathogens Á Enemy release hypothesis fungal pathogens attacking the seeds of both species in each country. The number of colonies of secondary

Introduction Communicated by Timothy Bell. Biological invasions are a primary threat to biodiver- K. Najberek (&) Á W. Solarz Á P. Olejniczak sity (Bellard et al. 2016; Spatz et al. 2017) and a Institute of Nature Conservation, Polish Academy of significant cause of economic losses (Vila` et al. 2010; Sciences, al. Adama Mickiewicza 33, 31-120 Krako´w, Poland Pimentel 2011). According to preliminary assess- e-mail: [email protected] ments, only 1% of alien species become invasive after introduction (Williamson and Fitter 1996) but since W. Pusz that work was done the figure has risen to 5–20% Department of Plant Protection, Wroclaw University of Environmental and Life Sciences, Plac Grunwaldzki 24A, (Jeschke 2014). For both the theory and practice of 53-363 Wrocław, Poland 123 1198 Plant Ecol (2018) 219:1197–1207 nature conservation, finding out which factors deter- balfourii may also be a result of its low popularity as mine the behavior of invasive species after they are an ornamental (Adamowski 2009), limiting its propag- introduced to new areas is an increasingly important ule pressure as compared with I. glandulifera. Another task (Simberloff and Rejma´nek 2011). suggestion offered is maladaptive habitat selection, as Vascular plants are the most intensively studied I. balfourii prefers roadsides where intensive mowing group of alien species (Pysˇek et al. 2009), and those of may create an ecological trap (Najberek et al. 2017). It the genus Impatiens hold a special place among them is also thought that the I. balfourii invasion may still be in view of their use as ornamentals, their high diversity in a lag phase, as it was introduced 60 years after the (more than 1000 species) and the occurrence of several invasive I. glandulifera (Adamowski 2009; Ugoletti spectacular invasions in different parts of the world et al. 2013). (Janssens et al. 2009; Vervoort et al. 2011). Despite the Another factor that may affect the invasiveness of large number of studies of alien Impatiens species alien species is lower pressure from local enemies (e.g., Kollmann and Ban˜uelos 2004; Adamowski such as predators, herbivores, or pathogens after 2008; Janssens et al. 2009; Ugoletti et al. 2011; introduction to new areas. Within their native range, Tanner et al. 2015; Jacquemart et al. 2015; Elst et al. species are suppressed by natural enemies. Liberation 2016), large questions remain, related to the great from this limiting factor in new areas may lead to rapid differences in invasiveness levels between closely spread. Studies of enemies of I. glandulifera in Europe related representatives of this genus introduced to the confirm that the species has been free of the impact of same region. generalist herbivores and pathogenic fungi (Burkhart Two such species are I. glandulifera and I. and Nentwig 2008). Impatiens balfourii has not been balfourii. The former is one of the most prominent tested in this respect yet, but it has been demonstrated invasive alien species in Europe (Drake 2009), which that level of its enemy release seems to depend on the resulted in introducing restrictions on its importation, habitat in which it occurs: plants growing along possession, and trade within European Union (Euro- roadsides were attacked less than those occurring pean Union Regulation 2014). Despite their close along streams, in forests and in ruderal areas (Najberek taxonomic relation (Janssens et al. 2009), I. balfourii is et al. 2017). non-invasive in Europe. Its rapid expansion and In this study we compared the levels of enemy negative impacts have been noted only in France, attack in these two Impatiens species within their Italy, and Croatia (Banfi and Galasso 2010; Fried et al. introduced range. We focused on the seeds. The 2014; EPPO 2018). The two species have been germination behavior of alien species may influence compared several times, and there is little evidence their invasiveness (Gioria and Pysˇek 2017), and it has that the performance of I. balfourii is worse than I. been shown that fungal pathogens decrease the vigor glandulifera. Their photosynthetic capacity and of seeds (e.g., the genera Fusarium or Rhizoctonia; growth rates are similar (Ugoletti et al. 2011). Both Leman´czyk and Sadowski 2002; Kordas et al. 2015; show high attractiveness to pollinators, self-compat- Pusz et al. 2016). One paper suggests that alien plants ibility, no effect of inbreeding depression (Jacquemart introduced to the United States from Europe are et al. 2015), high reproductive capacity (Ugoletti et al. infected by 84% fewer fungi than in their natural 2011; Jacquemart et al. 2015), allelopathic potential range, which may enhance their invasiveness (Mitch- (Vrchotova´ et al. 2011), and antimicrobial and ell and Power 2003). In this context it is odd that the antioxidant properties (Szewczyk et al. 2016). level of infestation of seeds has received little The low invasiveness of I. balfourii has been attention. Presumably this type of enemy release explained by its low frost tolerance (Perrins et al. would be particularly beneficial to annual plants such 1993; Tabak and von Wettberg 2008), which is as Impatiens, which disperse only by seeds. The particularly evident in mountain foothills where antimicrobial, antioxidant, and allelopathic abilities of differences in elevation are considerable (Najberek Impatiens make them particularly attractive study et al. 2017). If the species indeed suffers from frosts in subjects (Vrchotova´ et al. 2011; Csisza´r et al. 2012; Europe, its spread may increase in the future with Szewczyk et al. 2016). We hypothesized that seeds of climate warming (Schmitz and Dericks 2010; Naj- the highly invasive I. glandulifera would be less berek et al. 2017). However, the low invasiveness of I. 123 Plant Ecol (2018) 219:1197–1207 1199 attacked by fungi than seeds of the non-invasive I. Study area and seed collection balfourii in the introduced range of these species. Seeds of both species were collected in September 2016 in Insubria, a lake region on the border of Swiss Methods Ticino and Italian Lombardy in the foothills of the Southern Alps (Table 1; Fig. 1). The distribution of Species selected for study alien plants in the Alps is restricted, but the mild climate of the study area, a distinct bioclimatic region, Impatiens glandulifera Royle favors biological invasions (Berger and Walther 2006; Dainese et al. 2014; Najberek et al. 2017). Both of An annual plant introduced in 1839 to Europe from the these species are established there (Info Flora 2018). western Himalayas as an ornamental. The site of Impatiens balfourii was more widespread in Italy introduction was Kew Gardens in Great Britain, but than in Switzerland. We collected 2254 mature seeds the species extended its range beyond the British Isles of this species from four selected populations on the around 1900 (Valentine 1971; Helmisaari 2010). Italian side and from each of the only two populations Flowering occurs from June to October and seed set found in Switzerland. Impatiens glandulifera, on the has been noted to occur from late September. Impa- other hand, was more widespread in Switzerland. We tiens glandulifera disperses its seeds ballistically collected 1010 mature seeds from three of the Swiss (Helmisaari 2010; Jacquemart et al. 2015). In terms populations and from the only one found on the Italian of habitat preference it can be found in seminatural side (Table 1; Fig. 1). areas, including river valleys and forest edges, and its All six locations of I. balfourii were along roadsides adaptive abilities allow it to grow in highly altered – its most preferred habitat in Insubria (Najberek et al. ruderal habitats such as along roads or train tracks 2017). Each of the four locations of I. glandulifera was (Helmisaari 2010). in a different habitat: a wetland, a riverside, the Locarno airport urban area, and a roadside. Impatiens Impatiens balfourii Hook. f glandulifera was numerous in all surveyed habitats, and its seed weight suggested that the surveyed plants An annual plant introduced to Europe from the were in good condition (Table 1; Chmura et al. 2013). western Himalayas and Kashmir (Nasir 1980). It was The collected seeds were dried at room temperature cultivated first in France (Montpellier Botanic Gar- for two days and then stored in paper bags in room den) and Great Britain (Edinburgh Botanic Garden); temperature and transported to the laboratory of the escapes from cultivation have been noted since 1906 Department of Plant Protection, Wroclaw University (Adamowski 2009). The flower and seed morphology of Environmental and Life Sciences. A month later the of I. balfourii is similar to that of I. glandulifera, and it seeds were weighed to 0.001 g accuracy (PS 360.R2 disperses its seeds ballistically (Jacquemart et al. scale; Table 1) in controlled conditions. 2015). Flowering and seed set are also comparable to I. glandulifera and seed set occurs in the study area in Mycological analysis late September and October. In terms of habitat preference it may inhabit the same areas as I. To test whether the seed surfaces and cores were glandulifera (Ugoletti et al. 2013) but there are some attacked by fungal pathogens, mycological analyses differences: I. balfourii prefers a drier substrate, while were carried out between September and November I. glandulifera occurs in moist habitats (Schmitz and 2016. We randomly picked 360 seeds of each species: Dericks 2010). In Europe both species usually occur at 180 collected in Switzerland and 180 in Italy; the seeds elevations below 1000 m a.s.l., whereas in their native from particular localities were pooled within country. Himalayas I. balfourii grows at 1500–2500 m a.s.l. Ninety of each 180 seeds were placed directly on petri and I. glandulifera at 1800–4000 m a.s.l. (Nasir 1980; dishes with 2% solidified maltose, 10 seeds per dish. Adamowski 2009; Helmisaari 2010). The remaining 90 per group were disinfected with 1% sodium hypochlorite solution for 5 s and then treated as the previous group. Growing fungal colonies were 123 1200 Plant Ecol (2018) 219:1197–1207 identified to species level based on morphological Fig. 1 Localities of the sampled populations of Impatiens c characters. The type, color, and size of the mycelium glandulifera and I. balfourii on the Swiss–Italian border were determined. Then microscope slides were pre- pared so that the spores could be measured. Their size is one of the most important characters for species The number of fungal colonies per petri dish was identification (Pitt and Hocking 2009; Watanabe incorporated in the model as the response variable. 2011). Most frequently either one colony or none Since the number of colonies could exceed the number grew on a single seed. Two or more colonies were of seeds on the dish, the variable was assumed to be recorded occasionally. In those cases the shape of the Poisson-distributed, with the logarithm as the link colonies indicated unequivocally their independent function. The relationship between numbers of origin, so the number of colonies could be reliably colonies of fungal species was analyzed with the use assessed. The colonies of fungal taxa in each petri dish of Spearman non-parametric correlations. All statisti- were counted and summed. cal analyses employed SPSS ver. 24.0 (IBM Corp. Since our study focused on assessing the potential 2016). negative impact of enemies on seeds of both Impatiens species, we classified the recorded fungal species as true pathogens or secondary pathogens, and used only Results the former group in the tests. The group includes obligatory pathogens with invariably negative impacts The seeds were inhabited by 14 fungal species, 13 of on plants and their seeds, effects documented in the which were isolated from non-disinfected seeds literature (de Wit 2007). Secondary pathogens are (Table 2). Four of them were true pathogens of seeds: generally less harmful and in some circumstances their Fusarium culmorum, F. oxysporum, F. sporotri- presence may even benefit a plant by limiting its choides, and Giberella avenacea (Leman´czyk and infestation by true pathogens (Liggitt et al. 1997). Sadowski 2002; Schaafsma et al. 2005; Kordas et al. 2015; Gołe˛biowska et al. 2016; Pusz et al. 2016). Statistical analysis Disinfected seeds were attacked by only 6 species (Table 3), only one of which (Cladosporium her- The Impatiens species, country of origin, and seed barum) was not found earlier in the non-disinfected treatment (disinfected or non-disinfected) were used seeds. No true pathogens were found in disinfected as factors in a 2 9 2 9 2 full-factorial design. To test seeds. The most numerous fungal species in both for the differences between species and between treatments was C. cladosporioides. Both Cladospo- countries a generalized linear model (GLM) was used. rium species are considered to be secondary pathogens

Table 1 Localities, habitats, number of collected seeds and their average weight (AVG) in samples from Impatiens glandulifera and I. balfourii populations on the Swiss–Italian border Species Locality Habitat N seeds Mean seed weight (g)

I. glandulifera Switzerland, Bolle di Magadino Nature Reserve Wetland 60 0.010 Switzerland, Bolle di Magadino Nature Reserve Riverside 60 0.011 Switzerland, Locarno airport Airport 60 0.011 Italy, Germignaga Roadside 180 0.012 I. balfourii Switzerland, Monteggio Roadside 90 0.005 Switzerland, Ponte Brolla Roadside 90 0.004 Italy, near Musignano Roadside 45 0.004 Italy, Pino Sulla Sponda del Lago Maggiore Roadside 45 0.004 Italy, Pino Sulla Sponda del Lago Maggiore Roadside 45 0.004 Italy, Lavena Ponte Tresa Roadside 45 0.003

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Table 2 Number of Species I. glandulifera I. balfourii colonies of fungal species isolated from non- Switzerland Italy Switzerland Italy disinfected seeds of Impatiens glandulifera and Alternaria alternata 14 41 25 1 I. balfourii, collected in Aspergillus niger 0201 Switzerland and Italy Cladosporium cladosporioides 64 45 60 5 Epicoccum nigrum 5100 Fusarium culmorum 7000 Fusarium oxysporum 0012 Fusarium sporotrichoides 0001 Giberella avenacea 00628 Penicillium notatum 0307 Penicillium urticae 00240 Phoma leveillei 0100 Trichoderma harzianum 0006 Names of true pathogens Trichoderma viridae 0200 are bolded

Table 3 Number of Species I. glandulifera I. balfourii colonies of fungal species isolated from disinfected Switzerland Italy Switzerland Italy seeds of Impatiens glandulifera and I. Alternaria alternata 7102 balfourii, collected in Aspergillus niger 0003 Switzerland and Italy Cladosporium cladosporioides 14 0 7 8 Cladosporium herbarum 0600 Epicoccum nigrum 1000 Penicillium notatum 0018 and saprotrophs (Stone et al. 2000). Alternaria alter- Enemy attack assessments nata, Aspergillus niger, Phoma leveillei, Penicillium, and Trichoderma are also classified as secondary Only true pathogens (F. culmorum, F. oxysporum, F. pathogens (McRoberts and Lennard 1996; Stone et al. sporotrichoides, G. avenacea) were included in the 2000; Tekaia and Latge´ 2005; Aveskamp et al. 2008; tests. Overall, I. glandulifera seeds were less affected Pusz et al. 2016). than I. balfourii seeds by these fungi (B = 1.692, Correlation tests revealed that the number of p \ 0.001, df = 1). In seeds sourced from Italy, enemy colonies of C. cladosporioides (secondary pathogen, pressure was substantially higher on I. balfourii saprotroph) in non-disinfected seeds correlated nega- (B = - 1.488, p \ 0.001, df = 1, Fig. 2), while in tively with the combined number of colonies of true seeds sourced from Switzerland the level of enemy pathogen species (rS = - 0.528, p \ 0.001, N = 36). attack was similar for the two Impatiens species Moreover, the number of C. cladosporioides colonies (B = 0.000, NS, df = 1, Fig. 2). in non-disinfected seeds correlated positively with the number of colonies of another secondary pathogen, A. alternata (rS = 0.388, p \ 0.05, N = 36). Discussion

Among the many published tests of the influence of enemy pressure on alien plants invasion success there are only a few such studies of plant seeds. Blaney and 123 Plant Ecol (2018) 219:1197–1207 1203

the two alien species only in their introduced range and did not include native species. We expected the invasive alien species to be attacked by enemies at lower intensity than the non-invasive alien, an assumption similar to that of the ERH hypothesis which postulates that invasive alien species are under lower enemy pressure than native ones. True pathogens such as the Fusarium species recorded in our study significantly reduce the quality of seeds (Leman´czyk and Sadowski 2002; Kordas et al. 2015; Pusz et al. 2016). Giberella avenacea is another important true fungal pathogen of plants, harmful to seeds of various plant species (Schaafsma et al. 2005; Gołe˛biowska et al. 2016). We excluded the secondary and saprotrophic fungi from the tests Fig. 2 Mean number of true pathogen colonies per petri dish because their impact is uncertain; their presence can (± SE) recorded on non-disinfected seeds of Impatiens glan- be neutral or even beneficial to a plant, so they cannot dulifera and I. balfourii, sourced from Switzerland (CH) and Italy (IT) be automatically classified as enemies. For example, it is known that species of Cladosporium (the genus Kotanen (2001) used fungicide treatments to estimate most frequently found in our study) have negative the impact of soil fungi on seeds. They compared seed effects on seeds of many plant species (Waqas et al. germination success in natural soil and soil with added 2013) but that they help limit the occurrence of a much fungicide. Their results did not differ between alien more harmful genus – Fusarium (Liggitt et al. 1997). and native plant seeds. Beckstead and Parker (2003) The latter effect is supported by our finding of a used soil sterilization to test the effect of below- negative correlation between the occurrence of C. ground pathogens on seeds, comparing seed germina- cladosporioides and the occurrence of true pathogens. tion, seedling survival and the growth of the invasive The two Impatiens species we used to compare the alien Ammophila arenaria in its native European and level of pressure from true pathogens differ in their introduced North American range. They found that invasiveness. Thus, the success of the highly invasive seed germination and seedling survival decreased in I. glandulifera would be attributable to better release the non-sterilized soil, but no evidence of differences from enemies than the non-invasive I. balfourii.In in release from natural enemies between the two considering the between-country differences, how- ranges. They did, however, find that in the introduced ever, the dependence of invasiveness on the release range the seedlings and rhizosphere had no pathogenic from enemy pressure is less straightforward. In Italy, I. nematodes. Other studies have noted limiting effects balfourii was attacked by true pathogens substantially of soil pathogens on plant seedlings in their native more often than I. glandulifera was, while in Switzer- range (Packer and Clay 2000; Reinhart et al. 2003; land the seeds of the two species were under the same Callaway et al. 2004), suggesting that belowground level of pressure. It would seem that the assumption organisms may also affect invasion success. that invasive alien species are under lower enemy Our study concentrated on two alien Impatiens pressure than non-invasive ones was fully confirmed species that are closely related but surprisingly only on the Italian side of the border. different in their invasiveness in Europe. Impatiens This disparity could be a result of differences glandulifera is an invasive alien species, while I. between the communities of fungal pathogens that balfourii is non-invasive. In this respect our assess- colonized seeds of both species in Italy and Switzer- ment of the level of enemy attack broadens the land. It should be stressed that we isolated true traditional enemy release tests called for by the enemy pathogens only from non-disinfected seeds. This release hypothesis (ERH; Elton 1958; Maron and Vila` manifestation of pathogen resistance may reflect the 2001; Keane and Crawley 2002), because we studied antimicrobial, antioxidant, and/or allelopathic abilities of these plants (Vrchotova´ et al. 2011; Csisza´r et al. 123 1204 Plant Ecol (2018) 219:1197–1207

2012; Szewczyk et al. 2016). However, an alternative and were therefore less affected by maintenance work explanation can be inferred from our finding that the (e.g., in the Bolle di Magadino Nature Reserve). The I. number of colonies of the most numerous species, C. balfourii seeds from Switzerland were obtained cladosporioides, correlated negatively with the num- exclusively along roadsides. A difference in pathogen ber of colonies of true pathogens. This secondary abundance between the studied habitats may explain pathogen may have prevented the true pathogens from the lack of differences in infestation levels between the penetrating the seed core. Cladosporium cladospori- studied species on the Swiss side. In Italy, where the oides correlated positively with another secondary seeds of both species were collected from roadsides, pathogen, A. alternata, which has been found to the difference in the number of true pathogens on reduce the true pathogen F. culmorum (Liggitt et al. seeds was pronounced, with a lower level of attack on 1997). Both of these secondary pathogens may have the invasive I. glandulifera, supporting the assumption suppressed the true pathogens efficiently enough to of an inverse relation between enemy attack and keep the seed cores unaffected. It could also explain invasiveness. the contrasting ERH test results: non-disinfected seeds Seeds of I. balfourii were under the highest of I. balfourii from Italy were almost free of C. pathogen pressure in Italy. At the same time, however, cladosporioides or A. alternate; therefore the level of I. balfourii was more numerous on the Italian side enemy pressure in that case was highest; at the same (Najberek et al. 2017), so it may be that the impact of time, the number of colonies of both secondary the recorded true pathogens on these Impatiens seeds is pathogens was highest in Italian seeds of I. glandulif- not always as harmful as expected (Leman´czyk and era, and these seeds were not affected by true Sadowski 2002; Gołe˛biowska et al. 2016). It is worth pathogens at all. Moreover, the seeds of both species stressing that true pathogens were recorded only from collected on the Swiss side were under similar enemy non-disinfected seeds; the cores of the seeds of both pressure, a finding related to their comparable levels of Impatiens species were not affected. Further studies secondary pathogen occurrence. The reason for this would be required to find out whether the germination Swiss/Italian divergence of the fungal pathogen com- success of I. balfourii and I. glandulifera does depend munities is unclear. The big difference in the number on attack by true pathogens. Pathogens may decrease of colonies of C. cladosporioides and A. alternata was the viability of seeds already in the dormant stage but found for seeds of the Impatiens species collected also during germination. Germinating seed shells lose from the Italian roadsides. Swiss seeds of the two their integrity, and this may facilitate the penetration of species showed similar results for that parameter, pathogens to the core, affecting seedling performance. regardless of habitat, meaning that their levels of Tests of the influence of enemy attack on invasive- pathogen pressure probably did not depend on the type ness mainly compare the pressure exerted by enemies of habitat from which the seeds were collected. on native versus alien species; they pay less attention Another possible explanation for the disparate to the origin of these enemies (e.g., Tanner et al. 2015). results is that the two studied countries substantially A clear distinction between native and alien enemies differ in their road and green-area maintenance work would help to further clarify the evolution of plant- schemes. In Switzerland these areas are frequently pest interactions, but it is notoriously difficult to assess mowed and raked, and the cuttings are scrupulously the origin of small organisms, including pathogens. removed, all of which helps limit the invasion success Primary occurrence data are very scarce for many such of any alien plant species, especially annuals such as species, and their human-mediated transport to new Impatiens (Najberek et al. 2017). That maintenance areas is accidental and thus poorly documented work may also have a significant effect on the extent of (Pociecha et al. 2016; Solarz and Najberek 2017; true pathogen attack: the abundance of such pathogens Solarz et al. 2017). The origin of Fusarium oxyspo- in well-tended localities of I. balfourii in Switzerland rum, the true pathogen identified from Italian and could be lower. Impatiens glandulifera, the species Swiss I. balfourii seeds, seems open to question. It is more frequently found in Switzerland than in Italy, classified as an alien in Europe in the DAISIE database may have been exposed to relatively high levels of true (2018) but there are more than 120 different formae pathogens on the Swiss side, because the studied speciales of F. oxysporum (Michielse and Rep 2009) plants were collected mainly from less-mowed areas and probably only a few of them are not native to 123 Plant Ecol (2018) 219:1197–1207 1205

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